Supplementary files
.Transparent reporting form
DOI: https://doi.org/10.7554/eLife.38818.021
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files.
References
Abraham AD, Neve KA, Lattal KM. 2014. Dopamine and extinction: a convergence of theory with fear and reward circuitry.Neurobiology of Learning and Memory108:65–77.DOI: https://doi.org/10.1016/j.nlm.2013.
11.007,PMID: 24269353
Amano T, Duvarci S, Popa D, Pare´ D. 2011. The fear circuit revisited: contributions of the basal amygdala nuclei to conditioned fear.Journal of Neuroscience31:15481–15489.DOI: https://doi.org/10.1523/JNEUROSCI.3410-11.2011,PMID: 22031894
Badrinarayan A, Wescott SA, Vander Weele CM, Saunders BT, Couturier BE, Maren S, Aragona BJ. 2012.
Aversive stimuli differentially modulate real-time dopamine transmission dynamics within the nucleus accumbens core and shell.Journal of Neuroscience32:15779–15790.DOI: https://doi.org/10.1523/
JNEUROSCI.3557-12.2012,PMID: 23136417
Bayer HM, Glimcher PW. 2005. Midbrain dopamine neurons encode a quantitative reward prediction error signal.Neuron47:129–141.DOI: https://doi.org/10.1016/j.neuron.2005.05.020,PMID: 15996553
Beier KT, Steinberg EE, DeLoach KE, Xie S, Miyamichi K, Schwarz L, Gao XJ, Kremer EJ, Malenka RC, Luo L.
2015. Circuit architecture of vta dopamine neurons revealed by systematic input-output mapping.Cell162:
622–634.DOI: https://doi.org/10.1016/j.cell.2015.07.015,PMID: 26232228
Blanchard DC, Blanchard RJ. 1972. Innate and conditioned reactions to threat in rats with amygdaloid lesions.
Journal of Comparative and Physiological Psychology81:281–290.DOI: https://doi.org/10.1037/h0033521, PMID: 5084445
Bouton ME. 2004. Context and behavioral processes in extinction.Learning & Memory11:485–494.DOI: https://
doi.org/10.1101/lm.78804,PMID: 15466298
Bouton ME, Westbrook RF, Corcoran KA, Maren S. 2006. Contextual and temporal modulation of extinction:
behavioral and biological mechanisms.Biological Psychiatry60:352–360.DOI: https://doi.org/10.1016/j.
biopsych.2005.12.015,PMID: 16616731
Chang CY, Esber GR, Marrero-Garcia Y, Yau HJ, Bonci A, Schoenbaum G. 2016. Brief optogenetic inhibition of dopamine neurons mimics endogenous negative reward prediction errors.Nature Neuroscience19:111–116.
DOI: https://doi.org/10.1038/nn.4191,PMID: 26642092
Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, Looger LL, Svoboda K, Kim DS. 2013. Ultrasensitive fluorescent proteins for imaging neuronal activity.Nature 499:295–300.DOI: https://doi.org/10.1038/nature12354,PMID: 23868258
Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N. 2012. Neuron-type-specific signals for reward and punishment in the ventral tegmental area.Nature482:85–88.DOI: https://doi.org/10.1038/nature10754, PMID: 22258508
Craske MG, Stein MB, Eley TC, Milad MR, Holmes A, Rapee RM, Wittchen HU. 2017. Anxiety disorders.Nature Reviews Disease Primers3:17024.DOI: https://doi.org/10.1038/nrdp.2017.24,PMID: 28470168
den Ouden HE, Kok P, de Lange FP. 2012. How prediction errors shape perception, attention, and motivation.
Frontiers in Psychology3:548.DOI: https://doi.org/10.3389/fpsyg.2012.00548,PMID: 23248610
Duvarci S, Nader K. 2004. Characterization of fear memory reconsolidation.Journal of Neuroscience24:9269–
9275.DOI: https://doi.org/10.1523/JNEUROSCI.2971-04.2004,PMID: 15496662
Duvarci S, Pare D. 2014. Amygdala microcircuits controlling learned fear.Neuron82:966–980.DOI: https://doi.
org/10.1016/j.neuron.2014.04.042,PMID: 24908482
Eshel N, Bukwich M, Rao V, Hemmelder V, Tian J, Uchida N. 2015. Arithmetic and local circuitry underlying dopamine prediction errors.Nature525:243–246.DOI: https://doi.org/10.1038/nature14855,PMID: 26322583 Eshel N, Tian J, Bukwich M, Uchida N. 2016. Dopamine neurons share common response function for reward
prediction error.Nature Neuroscience19:479–486.DOI: https://doi.org/10.1038/nn.4239,PMID: 26854803 Felsenberg J, Jacob PF, Walker T, Barnstedt O, Edmondson-Stait AJ, Pleijzier MW, Otto N, Schlegel P, Sharifi N,
Perisse E, Smith CS, Lauritzen JS, Costa M, Jefferis G, Bock DD, Waddell S. 2018. Integration of parallel opposing memories underlies memory extinction.Cell175:709–722.DOI: https://doi.org/10.1016/j.cell.2018.
08.021,PMID: 30245010
Friston K. 2012. Prediction, perception and agency.International Journal of Psychophysiology83:248–252.
DOI: https://doi.org/10.1016/j.ijpsycho.2011.11.014,PMID: 22178504
Gentry RN, Lee B, Roesch MR. 2016. Phasic dopamine release in the rat nucleus accumbens predicts approach and avoidance performance.Nature Communications7:13154.DOI: https://doi.org/10.1038/ncomms13154, PMID: 27786172
Grace AA, Bunney BS. 1980. Nigral dopamine neurons: intracellular recording and identification with L-dopa injection and histofluorescence.Science210:654–656.DOI: https://doi.org/10.1126/science.7433992, PMID: 7433992
Graham BM, Milad MR. 2011. The study of fear extinction: implications for anxiety disorders.American Journal of Psychiatry168:1255–1265.DOI: https://doi.org/10.1176/appi.ajp.2011.11040557,PMID: 21865528 Groessl F, Munsch T, Meis S, Griessner J, Kaczanowska J, Pliota P, Kargl D, Badurek S, Kraitsy K, Rassoulpour A,
Zuber J, Lessmann V, Haubensak W. 2018. Dorsal tegmental dopamine neurons gate associative learning of fear.Nature Neuroscience21:952–962.DOI: https://doi.org/10.1038/s41593-018-0174-5,PMID: 29950668 Haaker J, Gaburro S, Sah A, Gartmann N, Lonsdorf TB, Meier K, Singewald N, Pape HC, Morellini F, Kalisch R.
2013. Single dose of L-dopa makes extinction memories context-independent and prevents the return of fear.
PNAS110:E2428–E2436.DOI: https://doi.org/10.1073/pnas.1303061110,PMID: 23754384
Herry C, Ciocchi S, Senn V, Demmou L, Mu¨ller C, Lu¨thi A. 2008. Switching on and off fear by distinct neuronal circuits.Nature454:600–606.DOI: https://doi.org/10.1038/nature07166,PMID: 18615015
Hikind N, Maroun M. 2008. Microinfusion of the D1 receptor antagonist, SCH23390 into the IL but not the BLA impairs consolidation of extinction of auditory fear conditioning.Neurobiology of Learning and Memory90:
217–222.DOI: https://doi.org/10.1016/j.nlm.2008.03.003,PMID: 18442937
Holtzman-Assif O, Laurent V, Westbrook RF. 2010. Blockade of dopamine activity in the nucleus accumbens impairs learning extinction of conditioned fear.Learning & Memory17:71–75.DOI: https://doi.org/10.1101/lm.
1668310,PMID: 20154351
Jin X, Costa RM. 2010. Start/stop signals emerge in nigrostriatal circuits during sequence learning.Nature466:
457–462.DOI: https://doi.org/10.1038/nature09263,PMID: 20651684
Jo YS, Heymann G, Zweifel LS. 2018. Dopamine Neurons Reflect the Uncertainty in Fear Generalization.Neuron 6273:30830–30834.DOI: https://doi.org/10.1016/j.neuron.2018.09.028
Lammel S, Hetzel A, Ha¨ckel O, Jones I, Liss B, Roeper J. 2008. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system.Neuron57:760–773.DOI: https://doi.org/10.1016/j.neuron.
2008.01.022,PMID: 18341995
Lammel S, Ion DI, Roeper J, Malenka RC. 2011. Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli.Neuron70:855–862.DOI: https://doi.org/10.1016/j.neuron.2011.03.025, PMID: 21658580
Lammel S, Steinberg EE, Fo¨ldy C, Wall NR, Beier K, Luo L, Malenka RC. 2015. Diversity of transgenic mouse models for selective targeting of midbrain dopamine neurons.Neuron85:429–438.DOI: https://doi.org/10.
1016/j.neuron.2014.12.036,PMID: 25611513
Lerner TN, Shilyansky C, Davidson TJ, Evans KE, Beier KT, Zalocusky KA, Crow AK, Malenka RC, Luo L, Tomer R, Deisseroth K. 2015. Intact-Brain Analyses Reveal Distinct Information Carried by SNc Dopamine Subcircuits.
Cell162:635–647.DOI: https://doi.org/10.1016/j.cell.2015.07.014,PMID: 26232229
Li W, Doyon WM, Dani JA. 2012. Quantitative unit classification of ventral tegmental area neurons in vivo.
Journal of Neurophysiology107:2808–2820.DOI: https://doi.org/10.1152/jn.00575.2011,PMID: 22378178 Luo R, Uematsu A, Weitemier A, Aquili L, Koivumaa J, McHugh TJ, Johansen JP. 2018. A dopaminergic switch
for fear to safety transitions.Nature Communications9:2483.DOI: https://doi.org/10.1038/s41467-018-04784-7,PMID: 29950562
Lynd-Balta E, Haber SN. 1994. The organization of midbrain projections to the striatum in the primate:
sensorimotor-related striatum versus ventral striatum.Neuroscience59:625–640.DOI: https://doi.org/10.1016/
0306-4522(94)90182-1,PMID: 7516506
Mahan AL, Ressler KJ. 2012. Fear conditioning, synaptic plasticity and the amygdala: implications for
posttraumatic stress disorder.Trends in Neurosciences35:24–35.DOI: https://doi.org/10.1016/j.tins.2011.06.
007,PMID: 21798604
Mahn M, Prigge M, Ron S, Levy R, Yizhar O. 2016. Biophysical constraints of optogenetic inhibition at presynaptic terminals.Nature Neuroscience19:554–556.DOI: https://doi.org/10.1038/nn.4266,PMID: 26 950004
Maren S, Phan KL, Liberzon I. 2013. The contextual brain: implications for fear conditioning, extinction and psychopathology.Nature Reviews Neuroscience14:417–428.DOI: https://doi.org/10.1038/nrn3492, PMID: 23635870
Matsumoto H, Tian J, Uchida N, Watabe-Uchida M. 2016. Midbrain dopamine neurons signal aversion in a reward-context-dependent manner.eLife5:e17328.DOI: https://doi.org/10.7554/eLife.17328,PMID: 27760002 Matsumoto M, Hikosaka O. 2009. Two types of dopamine neuron distinctly convey positive and negative
motivational signals.Nature459:837–841.DOI: https://doi.org/10.1038/nature08028,PMID: 19448610 Mayer D, Kahl E, Uzuneser TC, Fendt M. 2018. Role of the mesolimbic dopamine system in relief learning.
Neuropsychopharmacology43:1651–1659.DOI: https://doi.org/10.1038/s41386-018-0020-1,PMID: 29453443 Menegas W, Bergan JF, Ogawa SK, Isogai Y, Umadevi Venkataraju K, Osten P, Uchida N, Watabe-Uchida M.
2015. Dopamine neurons projecting to the posterior striatum form an anatomically distinct subclass.eLife4:
e10032.DOI: https://doi.org/10.7554/eLife.10032,PMID: 26322384
Menegas W, Babayan BM, Uchida N, Watabe-Uchida M. 2017. Opposite initialization to novel cues in dopamine signaling in ventral and posterior striatum in mice.eLife6:e21886.DOI: https://doi.org/10.7554/eLife.21886, PMID: 28054919
Menegas W, Akiti K, Amo R, Uchida N, Watabe-Uchida M. 2018. Dopamine neurons projecting to the posterior striatum reinforce avoidance of threatening stimuli.Nature Neuroscience21:1421–1430.DOI: https://doi.org/
10.1038/s41593-018-0222-1,PMID: 30177795
Milad MR, Quirk GJ. 2002. Neurons in medial prefrontal cortex signal memory for fear extinction.Nature420:
70–74.DOI: https://doi.org/10.1038/nature01138,PMID: 12422216
Milad MR, Quirk GJ. 2012. Fear extinction as a model for translational neuroscience: ten years of progress.
Annual Review of Psychology63:129–151.DOI: https://doi.org/10.1146/annurev.psych.121208.131631, PMID: 22129456
Morales M, Margolis EB. 2017. Ventral tegmental area: cellular heterogeneity, connectivity and behaviour.
Nature Reviews Neuroscience18:73–85.DOI: https://doi.org/10.1038/nrn.2016.165,PMID: 28053327 Mueller D, Bravo-Rivera C, Quirk GJ. 2010. Infralimbic D2 receptors are necessary for fear extinction and
extinction-related tone responses.Biological Psychiatry68:1055–1060.DOI: https://doi.org/10.1016/j.biopsych.
2010.08.014,PMID: 20926066
Myers KM, Davis M. 2007. Mechanisms of fear extinction.Molecular Psychiatry12:120–150.DOI: https://doi.
org/10.1038/sj.mp.4001939,PMID: 17160066
Nader K. 2015. Reconsolidation and the dynamic nature of memory.Cold Spring Harbor Perspectives in Biology 7:a021782.DOI: https://doi.org/10.1101/cshperspect.a021782,PMID: 26354895
Oleson EB, Gentry RN, Chioma VC, Cheer JF. 2012. Subsecond dopamine release in the nucleus accumbens predicts conditioned punishment and its successful avoidance.Journal of Neuroscience32:14804–14808.
DOI: https://doi.org/10.1523/JNEUROSCI.3087-12.2012,PMID: 23077064
Pape HC, Pare D. 2010. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear.Physiological Reviews90:419–463.DOI: https://doi.org/10.1152/physrev.00037.2009, PMID: 20393190
Parker NF, Cameron CM, Taliaferro JP, Lee J, Choi JY, Davidson TJ, Daw ND, Witten IB. 2016. Reward and choice encoding in terminals of midbrain dopamine neurons depends on striatal target.Nature Neuroscience 19:845–854.DOI: https://doi.org/10.1038/nn.4287,PMID: 27110917
Pitman RK, Rasmusson AM, Koenen KC, Shin LM, Orr SP, Gilbertson MW, Milad MR, Liberzon I. 2012. Biological studies of post-traumatic stress disorder.Nature Reviews Neuroscience13:769–787.DOI: https://doi.org/10.
1038/nrn3339,PMID: 23047775
Raczka KA, Mechias ML, Gartmann N, Reif A, Deckert J, Pessiglione M, Kalisch R. 2011. Empirical support for an involvement of the mesostriatal dopamine system in human fear extinction.Translational Psychiatry1:e12.
DOI: https://doi.org/10.1038/tp.2011.10,PMID: 22832428
Rescorla RA, Wagner AR. 1972. A theory of Pavlovian conditioning: variations in the effectiveness of
reinforcement and nonreinforcement. In: Black A. H, Prokasy W. F (Eds). In Classical Conditioning II: Current Research and Theory. Appleton-Century Crofts. p. 64–99.
Roeper J. 2013. Dissecting the diversity of midbrain dopamine neurons.Trends in Neurosciences36:336–342.
DOI: https://doi.org/10.1016/j.tins.2013.03.003,PMID: 23582338
Roesch MR, Calu DJ, Schoenbaum G. 2007. Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards.Nature Neuroscience10:1615–1624.DOI: https://doi.org/10.
1038/nn2013,PMID: 18026098
Schultz W, Dayan P, Montague PR. 1997. A neural substrate of prediction and reward.Science275:1593–1599.
DOI: https://doi.org/10.1126/science.275.5306.1593,PMID: 9054347
Schultz W, Dickinson A. 2000. Neuronal coding of prediction errors.Annual Review of Neuroscience23:473–500.
DOI: https://doi.org/10.1146/annurev.neuro.23.1.473,PMID: 10845072
Shi YW, Fan BF, Xue L, Wen JL, Zhao H. 2017. Regulation of Fear Extinction in the Basolateral Amygdala by Dopamine D2 Receptors Accompanied by Altered GluR1, GluR1-Ser845 and NR2B Levels.Frontiers in Behavioral Neuroscience11:116.DOI: https://doi.org/10.3389/fnbeh.2017.00116,PMID: 28676746
Soares S, Atallah BV, Paton JJ. 2016. Midbrain dopamine neurons control judgment of time.Science354:1273–
1277.DOI: https://doi.org/10.1126/science.aah5234,PMID: 27940870
Sotres-Bayon F, Quirk GJ. 2010. Prefrontal control of fear: more than just extinction.Current Opinion in Neurobiology20:231–235.DOI: https://doi.org/10.1016/j.conb.2010.02.005,PMID: 20303254
Steinberg EE, Keiflin R, Boivin JR, Witten IB, Deisseroth K, Janak PH. 2013. A causal link between prediction errors, dopamine neurons and learning.Nature Neuroscience16:966–973.DOI: https://doi.org/10.1038/nn.
3413,PMID: 23708143
Tian J, Uchida N. 2015. Habenula lesions reveal that multiple mechanisms underlie dopamine prediction errors.
Neuron87:1304–1316.DOI: https://doi.org/10.1016/j.neuron.2015.08.028,PMID: 26365765
Tovote P, Fadok JP, Lu¨thi A. 2015. Neuronal circuits for fear and anxiety.Nature Reviews Neuroscience16:317–
331.DOI: https://doi.org/10.1038/nrn3945,PMID: 25991441
Tsai HC, Zhang F, Adamantidis A, Stuber GD, Bonci A, de Lecea L, Deisseroth K. 2009. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning.Science324:1080–1084.DOI: https://doi.org/
10.1126/science.1168878,PMID: 19389999
Whittle N, Maurer V, Murphy C, Rainer J, Bindreither D, Hauschild M, Scharinger A, Oberhauser M, Keil T, Brehm C, Valovka T, Striessnig J, Singewald N. 2016. Enhancing dopaminergic signaling and histone acetylation promotes long-term rescue of deficient fear extinction.Translational Psychiatry6:e974.
DOI: https://doi.org/10.1038/tp.2016.231,PMID: 27922638
Wise RA. 2002. Brain reward circuitry: insights from unsensed incentives.Neuron36:229–240.DOI: https://doi.
org/10.1016/S0896-6273(02)00965-0,PMID: 12383779
Zhuang X, Masson J, Gingrich JA, Rayport S, Hen R. 2005. Targeted gene expression in dopamine and serotonin neurons of the mouse brain.Journal of Neuroscience Methods143:27–32.DOI: https://doi.org/10.1016/j.
jneumeth.2004.09.020,PMID: 15763133